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Complete genome sequence of Arcticibacterium luteifluviistationis SM1504T, a cytophagaceae bacterium isolated from Arctic surface seawater

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  • 1,
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  • 1,
  • 1, 2,
  • 1, 2,
  • 1, 2 and
  • 1Email author
Standards in Genomic Sciences201813:33

https://doi.org/10.1186/s40793-018-0335-x

  • Received: 21 July 2018
  • Accepted: 10 November 2018
  • Published:

Abstract

Arcticibacterium luteifluviistationis SM1504T was isolated from Arctic surface seawater and classified as a novel genus of the phylum Bacteroides. To date, no Arcticibacterium genomes have been reported, their genomic compositions and metabolic features are still unknown. Here, we reported the complete genome sequence of A. luteifluviistationis SM1504T, which comprises 5,379,839 bp with an average GC content of 37.20%. Genes related to various stress (such as radiation, osmosis and antibiotics) resistance and gene clusters coding for carotenoid and flexirubin biosynthesis were detected in the genome. Moreover, the genome contained a 245-kb genomic island and a 15-kb incomplete prophage region. A great percentage of proteins belonging to carbohydrate metabolism especially in regard to polysaccharides utilization were found. These related genes and metabolic characteristics revealed genetic basis for adapting to the diverse extreme Arctic environments. The genome sequence of A. luteifluviistationis SM1504T also implied that the genus Arcticibacterium may act as a vital organic carbon matter decomposer in the Arctic seawater ecosystem.

Keywords

  • Arcticibacterium luteifluviistationis
  • Secondary metabolite biosynthesis
  • Stress resistance
  • Carbohydrate metabolism
  • Arctic

Introduction

As the third most abundant bacterial group in the seawater system, phylum Bacteroidetes plays a vital role in diverse oceanic biogeochemical processes [1]. It has been reported that phylum Bacteroidetes could mediate the degradation of HMW compounds especially in the respect of algal organic matter [2, 3]. Many heterotrophic microorganisms such as the SAR11 clade and marine Gammaproteobacteria grow partly due to phylum Bacteroidetes -derived organic products [4, 5]. Thus, phylum Bacteroidetes groups may play crucial roles in the nutrient utilization and cycling in the seawater ecosystem.

The family Cytophagaceae , currently comprising 31 genera, is one of the largest groups in the phylum Bacteroidetes [6]. The species in the family Cytophagaceae have been isolated from various habitats including freshwater river [7], seawater [8], permafrost soil [9] and even polar glacial till [10]. The genus Arcticibacterium , belonging to the family Cytophagaceae , accommodates only one recognized species: A. luteifluviistationis SM1504T (=KCTC 42716T=CCTCC AB 2015348T) [11]. Strain SM1504T was isolated from surface seawater of King’s Fjord, Arctic. However, to date, no genomes of the genus Arcticibacterium have been reported, their genomic compositions and metabolic pathways are still lacking. In the study, we reported the first genome sequence of the genus Arcticibacterium to better understand its survival strategy and ecological niche in the Arctic seawater.

Organism information

Classification and features

As the type strain of A. luteifluviistationis in the family Cytophagaceae , strain SM1504T is a Gram-negative, aerobic, non-motile and rod bacterium (Fig. 1). The yellow-pigmented colony was found after incubation at 20 °C for 2 days on a TYS agar plate. The strain could utilize glycerol, D-xylose, D-glucose, D-fructose, dulcitol, inositol D-mannitol, D-sorbitol, N-acetylglucosamine, arbutin, aesculin, cellobiose, maltose, sucrose, trehalose, starch, turanose and potassium gluconate for energy and growth, which were summarized in Table 1. Then it hydrolyzed aesculin, gelatin, tyrosine, Tween 20, 40 and 60 but did not hydrolyze DNA, agar, casein, elastin, lecithin, starch, Tween 80. In addition, various enzymes such as alkaline phosphatase, esterase (C4), esterase lipase (C8), leucine arylamidase, valine arylamidase, cystine arylamidase, trypsin and glucosidase were produced for degrading organic matter [11]. The phylogenetic placement of strain SM1504T (based on complete 16S rRNA gene sequence) through neighbor-joining phylogenetic tree was identified (Fig. 2). It formed a distinct phylogenetic branch within the family Cytophagaceae and closely relatives were species of the genera Lacihabitans , Emticicia , Fluviimonas and Leadbetterella with low sequence similarities between 88.9 and 91.6%.
Fig. 1
Fig. 1

Transmission electron micrographs of Arcticibacterium luteifluviistationis SM1504T cultured on TYS broth medium. Scale bar, 0.5 μm

Table 1

Classification and general features of Arcticibacterium luteifluviistationis SM1504T [12]

MIGS ID

Property

Term

Evidence codea

 

Classification

Domain Bacteria

TAS [28]

  

Phylum Bacteroidetes

TAS [29, 30]

  

Class Cytophagia

TAS [30, 31]

  

Order Cytophagales

TAS [32, 33]

  

Family Cytophagaceae

TAS [32, 34]

  

Genus Arcticibacterium

TAS [11]

  

Species Arcticibacterium luteifluviistationis

TAS [11]

  

Strain: SM1504T

TAS [11]

 

Gram stain

Negative

TAS [11]

 

Cell shape

Rod

TAS [11]

 

Motility

Non-motile

TAS [11]

 

Sporulation

Not reported

 
 

Temperature range

4–30 °C

TAS [11]

 

Optimum temperature

20 °C

TAS [11]

 

pH range; Optimum

6.0–7.5; 6.5–7.0

TAS [11]

 

Carbon source

glycerol, D-xylose, D-glucose, D-fructose, dulcitol, inostiol D-mannitol, D-sorbitol, N-acetylglucosamine, arbutin, aesculin, cellobiose, maltose, sucrose, trehalose, starch, turanose and potassium gluconate

TAS [11]

MIGS-6

Habitat

seawater

TAS [11]

MIGS-6.3

Salinity

0–4% NaCl (w/v)

TAS [11]

MIGS-22

Oxygen requirement

Aerobic

TAS [11]

MIGS-15

Biotic relationship

Free-living

NAS

MIGS-14

Pathogenicity

Non-pathogen

NAS

MIGS-4

Geographic location

King’s Fjord, Arctic

TAS [11]

MIGS-5

Sample collection

2014

TAS [11]

MIGS-4.1

Latitude

Not reported

 

MIGS-4.2

Longitude

Not reported

 

MIGS-4.4

Altitude

Not reported

 

aEvidence codes -TAS Traceable Author Statement, NAS Non-traceable Author Statement. These evidence codes are from the Gene Ontology project [35]

Fig. 2
Fig. 2

Neighbor-joining phylogenetic tree based on 16S rRNA gene sequences, showing the relationships of Arcticibacterium luteifluviistationis SM1504T and its taxonomic neighbors. Rhodothermus marinus DSM 4252T was used as as the outgroup. Bootstrap values (> 70%) based on 1000 replicates are shown at nodes. Bar, 0.02 substitutions per nucleotide position

Genome sequencing information

Genome project history

Isolated from an extreme Arctic environment, A. luteifluviistationis SM1504T was selected for genome sequencing to elucidate the special abilities of adapting to diverse extreme stresses. We have accomplished the genome sequencing of strain SM1504T as reported in this paper. The complete genome data has been deposited in the GenBank database under the accession number CP029480.1. The project information and its association with MIGS are provided in Table 2 [12].
Table 2

Project information

MIGS ID

Property

Term

MIGS 31

Finishing quality

Complete

MIGS-28

Libraries used

Two genomic libraries: one Illumina library, one PacBio standard library

MIGS 29

Sequencing platforms

Illumina Hiseq 2500, PacBio RS

MIGS 31.2

Fold coverage

315× Illumina, 45× PacBio

MIGS 30

Assemblers

SOAPdenovo v. 2.04; HGAP v. 2.3.0

MIGS 32

Gene calling method

Prodigal

Locus Tag

SM1504

Genbank ID

CP029480.1

GenBank Date of Release

June 20, 2018

GOLD ID

Not registered

BIOPROJECT

PRJNA471374

MIGS 13

Source Material Identifier

KCTC 42716T=CCTCC AB 2015348T

Project relevance

Environmental, microbes

Growth conditions and genomic DNA preparation

A. luteifluviistationis SM1504T was cultivated in TYS broth at 20 °C. After cultivation for two days, genomic DNA for sequencing was extracted by using a commercial bacterial DNA isolation kit (OMEGA).

Genome sequencing and assembly

Genome sequencing was performed on both the Illumina Hiseq and the PacBio RS sequencing platforms. 400-bp Illumina paired-end libraries and 20-kb PacBio libraries were constructed and sequenced yielding 315 × and 45 × average coverages, respectively (Table 2). About 1.69 Gb and 243 Mb data from the Illumina and PacBio sequencing were assembled using SOAPdenovo [13, 14] and HGAP [15]. The final assembly resulted in one scaffold.

Genome annotation

Coding gene sequences were predicted and annotated through Prodigal v2.6.3 [16] and RAST v2.0 [17]. Functional categorization and carbohydrate-active enzymes CAZy of the predicted genes were annotated against EggNOG and CAZy databases, respectively. Then rRNAs and tRNAs were predicted by RNAmmer v1.2 [18] and tRNAscan-SE v1.3.1 [19]. In addition, the CARD analyses were performed to find resistance genes. Genomic islands and secondary metabolite biosynthesis were predicted through IslandViewer 4 [20] and antiSMASH [21].

Genome properties

The total size of the genome of A. luteifluviistationis SM1504T is 5,379,839 bp with an average GC content of 37.20% (Fig. 3). Total 4595 protein-coding genes (CDSs) were identified, which occupied 89.73% of the genome. Therein, 3045 CDSs were annotated with putative functions and 1550 CDSs matched hypothetical proteins (Table 3). Then 4 rRNAs and 36 tRNAs were found in the genome. CRISPR repeat, transmembrane helice, signal peptide and Pfam protein family predictions were done. In addition, distribution of genes into COG functional categories was shown in Table 4.
Fig. 3
Fig. 3

Circular map of the Arcticibacterium luteifluviistationis SM1504T genome. From the outside to the center: CDSs on forward strand (colored by COG categories), CDSs on reverse strand (colored by COG categories), RNA genes (tRNAs and rRNAs), G + C content and GC skew

Table 3

Genome statistics

Attribute

Value

% of Total

Genome size (bp)

5,379,839

100

DNA coding (bp)

4,827,135

89.73

DNA G + C (bp)

2,029,275

37.20

DNA scaffolds

1

100.00

Total genes

4635

100.00

Protein coding genes

4595

99.14

RNA genes

40

0.86

Pseudo genes

0

0

Genes in internal clusters

NA

NA

Genes with function prediction

3045

65.70

Genes assigned to COGs

3319

71.61

Genes with Pfam domains

3617

78.04

Genes with signal peptides

693

14.95

Genes with transmembrane helices

988

21.32

CRISPR repeats

4

0.09

NA, not applicable

Table 4

Number of genes associated with general COG functional categories

Code

Value

%age

Description

J

148

3.19

Translation, ribosomal structure and biogenesis

A

0

0

RNA processing and modification

K

180

3.88

Transcription

L

121

2.61

Replication, recombination and repair

B

0

0

Chromatin structure and dynamics

D

17

0.37

Cell cycle control, Cell division, chromosome partitioning

V

68

1.47

Defense mechanisms

T

154

3.32

Signal transduction mechanisms

M

273

5.89

Cell wall/membrane biogenesis

N

3

0.06

Cell motility

U

29

0.63

Intracellular trafficking and secretion

O

129

2.78

Posttranslational modification, protein turnover, chaperones

C

201

4.34

Energy production and conversion

G

229

4.94

Carbohydrate transport and metabolism

E

211

4.55

Amino acid transport and metabolism

F

68

1.47

Nucleotide transport and metabolism

H

83

1.79

Coenzyme transport and metabolism

I

85

1.83

Lipid transport and metabolism

P

224

4.83

Inorganic ion transport and metabolism

Q

45

0.97

Secondary metabolites biosynthesis, transport and catabolism

R

0

0

General function prediction only

S

1080

23.30

Function unknown

1286

27.75

Not in COGs

The total is based on the total number of protein coding genes in the genome

Insights from the genome sequence

Adaption to diverse stresses

Strain SM1504T genome owned two putative gene clusters for secondary metabolite biosynthesis. The cluster 1 belonged to terpene type - the largest group of natural products [22], matching the carotenoid biosynthesis. The cluster 2, affiliated to arylpolyene type, was predicted to produce flexirubin. Furthermore, we found that the yellow-pigmented strain SM1504T harbors a complete set of genes required for zeaxanthin biosynthesis (e.g., isopentenyl-diphosphate delta-isomerase, phytoene synthase, phytoene dehydrogenase, lycopene cyclase and beta-carotene hydroxylase), which was commonly detected in other species of the phylum Bacteroidetes [23, 24]. The pigment maybe help the strain to obtain energy and for cold adaption and ultraviolet light protection in the Arctic environments [25].

A total of 150 resistance genes were found to encode 24 kinds of antibiotics (such as gentamicin, kanamycin, tetracycline and streptomycin), which was consistent with the experimental antibiotic susceptibility results [11]. The genes encoding heat shock proteins dnaK and cold shock protein cspA were detected in the genome. In line with this, SM1504T had a wider growth temperature ranges (4–30 °C) [11]. Besides, the genome harbored several genes coding for catalase and superoxide dismutase to assist the strain at cellular and molecular levels in dealing harsh radiation in the Arctic. Dozens of genes related to osmotic stress (such as choline and betaine uptake and betaine biosynthesis) and carbon starvation responses were discovered in the A. luteifluviistationis genome, which would endow cells with tolerance to hyperhaline and oligotrophic environments.

As another feature, a 245-kb genomic island coding for 208 genes was predicted. Therein, 9 genes encoded proteins related to glucide biosynthesis, such aslipopolysaccharide core biosynthesis glycosyltransferase (lpsD), UDP-glucose dehydrogenase and capsular polysaccharide synthesis enzyme (Cap8C). In addition, the presence of transposases, integrases and mobile element proteins indicated that gene transfer has occurred in the A. luteifluviistationis SM1504T genome [26]. Also, phage tail fiber proteins were predicted, which was in line with the analysis by PHAST [27] that a 15-kb incomplete prophage region could encode phage tail fiber proteins in the genome.

Degradation and utilization of carbohydrates

Totally, 3319 (71.61%) genes could be assigned a COG function, of which the wall/membrane/envelope biogenesis (5.89%), carbohydrate transport and metabolism (4.94%) and inorganic ion transport and metabolism (4.83%) were enriched (Table 4). The high percentage of proteins related to carbohydrate transport and metabolism suggested that the strain SM1504T could use various carbohydrates. On the other hand, the analyses from dbCAN showed that the strain SM1504T possessed 341 genes which encoded carbohydrate metabolism enzymes, including 69 carbohydrate esterases (11 families), 125 glycoside hydrolases (46 families), 62 glycosyltransferases (22 families), 17 polysaccharide lyases (6 families), 12 auxiliary activities (3 families) and 56 carbohydrate-binding modules (15 families). Therein, a variety of enzymes are related to the degradation of macromolecular polysaccharides (e.g., xylanase, chitinase, mannanase, alpha amylase, endoglucanase, glucoamylase and alginate lyase) derived from marine macroalgae and phytoplankton. Those polysaccharases could hydrolyze a variety of macromolecular polysaccharides into small molecules that can be absorbed and metabolized by strain SM1504T and other microorganisms in the seawater [4, 5].

Conclusions

The genomic analyses showed that the strain SM1504T could adapt to extreme Arctic seawater environments, such as high solar radiation, cold temperature and high salinity. Besides, it may act as a vital macromolecular polysaccharide decomposer and would play an important role in organic carbon cycling in the Arctic seawater ecosystem.

Abbreviations

CARD: 

Comprehensive antibiotic resistance database

CAZy: 

Carbohydrate-active enzymes

CRISPR: 

Clustered regularly interspaced short palindromic repeats

HMW: 

High molecular weight

MIGS: 

Minimum information on the genome sequence

RAST: 

Rapid annotation using subsystem technology

TYS: 

Tryptone-yeast extract-sea salt

Declarations

Funding

This work was supported by the National Science Foundation of China (31670063, 31670038, 31630012 and 31770412), AoShan Talents Cultivation Program Supported by Qingdao National Laboratory for Marine Science and Technology (2017ASTCP-OS14), the Program of Shandong for Taishan Scholars (TS20090803), the Science and Technology Basic Resources Investigation Program of China (2017FY100804), the National Postdoctoral Program for Innovative Talents (BX201700145), the funding from key laboratory of global change and marine-atmospheric chemistry of the state oceanic administration (2018GCMAC16), Young Scholars Program of Shandong University (2016WLJH36).

Authors’ contributions

YL and PW conducted the main tasks, including experiments, genomic analysis and manuscript writing. XHG and YRD performed phylogenetic analysis. QLQ provided technical support for this study. XYZ and XLC helped to revise the manuscript. All authors read and approved the final manuscript.

Competing interests

The authors declare that they have no competing interests.

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Authors’ Affiliations

(1)
State Key Laboratory of Microbial Technology, Marine Biotechnology Research Center, Shandong University, No.72, Binhai Rd, Qingdao, 266237, China
(2)
Laboratory for Marine Biology and Biotechnology, Qingdao National Laboratory for Marine Science and Technology, No.1, Wenhai Rd, Qingdao, 266237, China

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Copyright

© The Author(s). 2018

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